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This is a repository copy of Delayed meal timing after exercise is associated with reduced

appetite and energy intake in adolescents with obesity.

White Rose Research Online URL for this paper:

https://eprints.whiterose.ac.uk/168421/

Version: Accepted Version

Article:

Fillon, A, Beaulieu, K orcid.org/0000-0001-8926-6953, Miguet, M et al. (8 more authors)

(2020) Delayed meal timing after exercise is associated with reduced appetite and energy

intake in adolescents with obesity. Pediatric Obesity, 15 (9). e12651. ISSN 2047-6310

https://doi.org/10.1111/ijpo.12651

© 2020 World Obesity Federation. This is the peer reviewed version of the following

article: Fillon, A, Beaulieu, K, Miguet, M, et al. Delayed meal timing after exercise is

associated with reduced appetite and energy intake in adolescents with obesity. Pediatric

Obesity. 2020; 15:e12651. , which has been published in final form at

https://doi.org/10.1111/ijpo.12651. This article may be used for non-commercial purposes

in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions.

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Delayed meal timing after exercise is associated with reduced appetite and

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energy intake in adolescents with obesity

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Abstract

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Background. While the beneficial effects of exercise on appetite might depend on its timing during

5

the day or relative to a meal, this remains poorly explored in youth. 6

Objectives. To examine the importance of meal timing (+30vs.+90minutes) after performing exercise

7

on energy intake, appetite and food reward in adolescents with obesity. 8

Methods. Eighteen adolescents with obesity randomly completed 3 conditions: i) lunch (12:00pm) set 9

30min after a rest session (11:00am); ii) lunch (12:00pm) set 30min after an exercise session (11:00 10

am)(MEAL-30); iii) lunch (01:00pm) set 90min after an exercise session (11:00am)(MEAL-90). Lunch 11

and dinner ad libitum energy intake was assessed, food reward (LFPQ) assessed before and after lunch, 12

and before dinner, appetite sensations were assessed at regular intervals. 13

Results. Energy intake was lower at MEAL-90 than MEAL-30 and CON at lunch (p<0.05 and p<0.01, 14

respectively) and lunch+dinner combined(p<0.001). A decrease in intake (g) of protein, fat and 15

carbohydrate was observed. Post-exercise hunger was lower on MEAL-90 compared with CON. No 16

condition effects were found at lunch for food reward. 17

Conclusions. Delaying the timing of the meal after exercise might help affect energy balance by 18

decreasing ad libitum energy intake without increasing hunger and by improving satiety in adolescents 19

with obesity. 20

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Key words. Exercise Timing, Appetite, Energy Intake, Obesity, Adolescent, Food reward

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Clinical Trial reference: NCT03968458

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2 24

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Introduction

25

While practitioners and clinicians constantly work on the improvement of their weight loss 26

interventions, trying to identify the best exercise characteristics (modality, intensity, duration, etc.) to 27

prescribe, the need to also consider the timing of exercise has been recently suggested 1. Recent

28

studies effectively show that the beneficial effects of exercise might also depend on its timing during 29

the day or its delay/position regarding a meal 1. Some studies for instance showed that performing

30

acute exercise one to three hours after a meal could enhance the glycemic response in patients with 31

type II diabetes 2–5 while others showed a better postprandial lipemia response when exercise was

32

performed immediately before the meal 6–8.

33

Looking at the alarming progression of overweight and obesity among children and adolescents, it 34

seems necessary to deepen our understanding on the effects of exercise on overall energy balance, in 35

order to optimize our weight loss strategies. It is now clear that physical exercise does not only impact 36

energy expenditure, it also affects energy intake and appetite control in youth and adolescents with 37

obesity 9. The current literature mainly investigated the effect of exercise duration 10,11, intensity 12–14

38

or modality 15 on subsequent food intake, appetite sensations or food reward, while the potential role

39

played by the timing of exercise remains poorly explored 16.

40

In 2017, Mathieu and collaborators assessed the effects of exercising immediately before or after a 41

lunch meal in primary school children on overall energy balance 17. Although they did not observe any

42

difference on energy intake between conditions (before or after the meal), their results highlight the 43

beneficial effect of performing pre-meal moderate-to-vigorous over low-intensity exercise on 44

subsequent energy intake 17. More recently, similar results were obtained among adolescents with

45

obesity whose energy intake and food reward remained unchanged whether the adolescents 46

performed 30 min of cycling exercise (65% VO2peak) immediately before or after their lunch meal 18.

47

Interestingly, others investigated the potential effect of the delay between an acute exercise bout and 48

the following meal on energy intake and appetite. In their work, Albert and colleagues compared the 49

effects of exercising (treadmill running at 70% VO2max) 45 min or 180 min before lunch, in normal

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4 weight adolescents 19. The authors observed an 11% reduction of the adolescents’ ad libitum energy

51

intake and a 23% decrease in fat intake when the exercise was performed 45 min before lunch, 52

compared to 180 min. Moreover, there were no difference in terms of appetite sensations and no 53

energy compensation at the following snack or dinner. Our research group recently examined the 54

effect of the exercise-meal delay on energy intake, appetite and food reward among adolescents with 55

obesity 20. According to our results, a 30-min cycling exercise bout (65% VO

2max) performed 60 min

56

before lunch favored a 14% reduction of ad libitum energy intake while the same exercise performed 57

180 min before lunch did not affect the adolescents’ energy intake. While appetite sensations (hunger, 58

fullness, prospective food consumption and desire to eat) did not differ between conditions, our 59

results also showed a significantly lower pre-meal explicit liking for high-fat relative to low-fat foods 60

when the exercise was set close to the meal, suggesting the implication of the food reward system 20.

61

Altogether, these results seem to show a beneficial effect of exercising close to a meal on overall 62

energy balance in adolescents. 63

Although these studies compared exercises of similar characteristics (e.g. duration, modality, 64

intensity), their metabolic demand might have been different due to their divergent delay from 65

breakfast, which might have important implications when it comes to subsequent energy intake. 66

Indeed, it has been shown that the metabolic activity during exercise, particularly the contribution of 67

the energy substrates, is different depending on the delay between a breakfast and this exercise 21.

68

The substrate oxidation during exercise, especially the rate of carbohydrate oxidation has been 69

associated with subsequent energy intake 22, particularly in adults with obesity 23,24. Investigating the

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effect of the timing of exercise on appetite and energy intake needs to consider not only its delay with 71

the following meal but also the time interval between exercise and the previous food intake. 72

In that context, the aim was to examine the importance of meal timing (+30 or +90 minutes) after 73

performing exercise on energy intake, appetite and food reward in adolescents with obesity. 74

75

Materials and methods

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5

Participants

77

Eighteen adolescents with obesity (according to 25) aged 12-15 years (Tanner stage 3-4) were enrolled

78

in this study (12 boys (12.6 ± 1.2 years) and 6 girls (13.0 ± 1.6 years)). They were recruited through the 79

local Pediatric Obesity Center (Tza Nou, La Bourboule, France), based on the following main inclusion 80

criteria: i) to be free of any medication known to influence appetite or metabolism; ii) to be free of 81

any contraindication to physical activity; iii) to be classified as physically inactive (taking part in less 82

than 2 hours of physical activity per week as assessed using the International Physical Activity 83

Questionnaire –IPAQ 26). This study was conducted in accordance with the Helsinki declaration and all

84

the adolescents and their legal representative received information sheets and signed consent forms 85

as requested by the local ethical authorities (Human Ethical Committee authorization reference: 2019-86

A00530-57; Clinical Trial reference: NCT03968458). 87

1.1. Design

88

After a preliminary medical inclusion visit performed by a pediatrician to control for the ability of the 89

adolescents to complete the study, they were asked to perform a maximal aerobic test and their body 90

composition was assessed by dual-energy x-ray absorptiometry (DXA). The adolescents thereafter 91

completed the three following experimental sessions (one week apart) in randomized order: i) lunch 92

(at 12:00pm) set 30 min after a rest session (at 11:00 am) ii) lunch (at 12:00pm) set 30 min after an 93

exercise session (at 11:00am; MEAL-30); iii) lunch (at 1:00pm) set 90 min after an exercise session (at 94

11:00am; MEAL-90). On the three occasions, participants received a standardized breakfast (08:00am) 95

and were asked to remain at rest (CON) or to cycle for 30 min at 11:00am and eat either 30 min (on 96

MEAL-30; lunch at 12:00pm) or 90 min (on MEAL-90; lunch at 1:00pm) after exercise. Dinner was 97

provided to the adolescents at 6:30pm. They were asked to complete the Leeds Food Preference 98

Questionnaire (LFPQ) 27 before and after the lunch meal and before dinner. Lunch and dinner energy

99

intake were assessed via ad libitum buffet-style meals. Appetite sensations were measured at regular 100

intervals throughout the day. Outside the experimental conditions and between the two ad libitum 101

test meals, the adolescents stayed in the laboratory, devoid of any food cues, and were requested not 102

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6 to engage in any moderate-to-vigorous physical activity and mainly completed sedentary activities 103

such as reading, homework or board games. Figure 1 details the whole design of the study. 104

………Figure 1……….. 105

1.2. Anthropometric characteristics and body composition

106

Body mass and height were measured wearing light clothing while bare-footed, using a digital scale 107

and a standard wall-mounted stadiometer, respectively. Body mass index (BMI) was calculated as 108

body mass (kg) divided by height squared (m²) and the sex and age dependent French reference curves 109

were used to obtain the BMI percentile 28. Fat mass (FM) and fat-free mass (FFM) were assessed by

110

dual-energy X-ray absorptiometry (DXA) following standardized procedures (QDR4500A scanner, 111

Hologic, Waltham, MA, USA). These measurements were obtained during the preliminary visit by a 112

trained technician. 113

1.3. Peak oxygen uptake test (V̇O2peak)

114

Each adolescent performed a V̇O2peak test on a traditional ergometer 29. The initial power was set at

115

30W during 3 minutes, followed by a 15W increment every minute until exhaustion. The adolescents 116

were strongly encouraged by the experimenters throughout the test to perform their maximal effort. 117

Maximal criteria were: heart rate >90% of the theoretical maximum heart rate (210 − 0.65 × age), 118

respiratory exchange ratio (RER = V̇CO2/V̇O2) > 1.1 and/or V̇O2 plateau. Cardiac electrical activity

119

(Ultima SeriesTM, Saint Paul, MN) and heart rate (Polar V800) were monitored and the test was 120

coupled with a measurement of breath-by-breath gas exchanges (BreezeSuite Software, Saint Paul, 121

MN), that determined V̇O2 and V̇CO2. Volumes and gases were calibrated before each test. V̇O2peak was

122

defined as the average of the last 30 s of exercise before exhaustion. 123

1.4. Experimental conditions

124

Rest condition (CON): During this condition, the adolescents were asked to remain quiet and were not

125

allowed to engage in any physical activity. They were asked to stay seated on a comfortable chair (30 126

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7 min) between 11:00am and 11:30am, not being allowed to talk, read, watch TV or to complete any 127

intellectual tasks. Energy expenditure was assessed during the 30-min rest period using portable 128

indirect calorimetry (K4b², COSMED Inc., Rome, Italy). 129

Lunch condition 30 min after exercise (MEAL-30): Between 11:00am and 11:30am, the participants

130

performed a 30-min moderate-intensity exercise bout (65% VO2peak) on a cycle ergometer. The

131

intensity was controlled by heart rate records (Polar V800) using the results from the maximal aerobic 132

capacity testing. Exercise-induced energy expenditure was calculated based on the results obtained 133

during the maximal oxygen uptake test. 134

Lunch condition 90 min after exercise (MEAL-90): The adolescents performed the same exercise bout

135

as MEAL-30 and at the same time, but the ad libitum lunch meal was served at 1:00pm (90 min after 136

the end of the exercise). 137

1.5. Energy intake

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At 08:00am, the adolescents consumed a standardized calibrated breakfast (500 kcal) respecting the 139

recommendations for their age (composition: bread (50 g), butter (10 g), marmalade (15 g), yoghurt 140

(125 g) or semi-skimmed milk (20 cl), fruit or fruit juice (20 cl)). Lunch and dinner meals were served 141

ad libitum using a buffet-type meal. The content of the buffets was determined using a food

142

preference and habits questionnaire filled in by the adolescents during the inclusion visit, as previously 143

described 30. Top rated items as well as disliked items and items liked but not usually consumed were

144

excluded to avoid over-, under- and occasional consumption. The lunch menu was beef steak, pasta, 145

mustard, cheese, yoghurt, compote, fruits and bread. The dinner menu was ham/turkey, beans, 146

mashed potato, cheese, yoghurt, compote, fruits and bread. Food items were presented in abundance 147

and the adolescents were told to eat until comfortably full. Adolescents made their choices and 148

composed their trays individually before joining their habitual table (5 adolescents per table). Lunch 149

and dinner were served in a quiet environment free of music, cellphones or television. Food items 150

were weighed by the experimenters before and after each meal. Energy intake and macronutrient 151

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8 composition (proportion of fat, carbohydrate and protein) were calculated using the software Bilnut 152

4.0. This methodology has been previously validated and published 30. Lunch and total relative energy

153

intake (REI) were calculated such as: energy intake – exercise-induced energy expenditure. 154

1.6. Subjective appetite sensations

155

Appetite sensations were collected at regular intervals throughout the day using visual analogue scales 156

(150-mm scales) 31. Adolescents had to report their hunger, fullness, desire to eat (DTE) and

157

prospective food consumption (PFC) before and immediately after breakfast, prior and after rest 158

(CON) or exercise (MEAL-30 and MEAL-90), before and immediately after lunch, 30 min and 60 min 159

after lunch, before and immediately after dinner. 160

1.7. Food liking and wanting

161

The Leeds Food Preference Questionnaire, described in greater methodological detail by Dalton and 162

Finlayson 32, provided measures of food preference and food reward. The adolescents were presented

163

with a culturally (food items and language) adapted version of the LFPQ following the recent 164

recommendations from Oustric and collaborators 33. Participants were presented with an array of

165

pictures of individual food items common in the diet. Foods were chosen by the local research team 166

from a validated database to be either predominantly high (>50% energy) or low (<20% energy) in fat 167

but similar in familiarity, protein content, palatability and suitable for the study population. The LFPQ 168

has been deployed in a range of research 32 including a recent exercise/appetite trial in young French

169

males 34 and adolescents 20,35,36.

170

Explicit liking was measured by participants rating the extent to which they like each food (“How 171

pleasant would it be to taste this food now?”). The food images were presented individually, in a 172

randomized order and participants made their ratings using a 100-mm VAS. Implicit wanting was 173

assessed using a forced choice methodology in which the food images were paired so that every image 174

from each of the four food types was compared to every other type over 96 trials (food pairs). 175

Participants were instructed to respond as quickly and accurately as they could to indicate the food 176

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9 they want to eat the most at that time (“Which food do you most want to eat now?”). Reaction times 177

for all responses were covertly recorded and used to compute mean response times for each food 178

type after adjusting for frequency of selection. 179

Responses on the LFPQ were used to compute mean scores for high-fat, low-fat, sweet or savoury 180

food types (and different fat-taste combinations). Fat bias scores were calculated as the difference 181

between the high-fat scores and the low-fat scores, with positive values indicating greater liking or 182

wanting for high-fat relative to low-fat foods and negative values indicating greater liking or wanting 183

for low-fat relative to high-fat foods. Sweet bias scores were calculated as the difference between the 184

sweet and savoury scores, with positive values indicating greater liking or wanting for sweet relative 185

to savoury foods and negative values indicating greater liking or wanting for savoury relative to sweet 186

foods. 187

1.8. Statistical analysis

188

Statistical analyses were performed using Stata software, Version 13 (StataCorp, College Station, TX, 189

US). The sample size estimation was determined according to (i) CONSORT 2010 statement, extension 190

to randomized pilot and feasibility trials (Eldridge et al. CONSORT 2010 statement: extension to 191

randomized pilot and feasibility trials. Pilot and Feasibility Studies (2016) 2:64) and (ii) Cohen’s 192

recommendations 37 who has defined effect-size bounds as : small (ES: 0.2), medium (ES: 0.5) and large

193

(ES: 0.8, “‘grossly perceptible and therefore large”). So, with 15 patients by condition, an effect-size 194

around 1 can be highlighted for a two-sided type I error at 1.7% (correction due to multiple 195

comparisons), a statistical power greater than 80% and an intra-class correlation coefficient at 0.5 to 196

take into account between and within participant variability. All tests were two-sided, with a Type I 197

error set at 0.05. Continuous data was expressed as mean ± standard deviation (SD) or median 198

[interquartile range] according to statistical distribution. The assumption of normality was assessed 199

by using the Shapiro-Wilk test. Daily (total) area under the curve (AUC) were calculated using the 200

trapezoidal method. Random-effects models for repeated data were performed to compare three 201

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10 conditions (i) considering the following fixed effects: time, condition and time x condition interaction, 202

and (ii) taking into account between and within participant variability (subject as random-effect). A 203

Sidak’s type I error correction was applied to perform multiple comparisons. As proposed by some 204

statisticians 38,39 a particular focus will be also given to the magnitude of differences, in addition to

205

inferential statistical tests expressed using p-values. The normality of residuals from these models was 206

studied using the Shapiro-Wilk test. When appropriate, a logarithmic transformation was proposed to 207

achieve the normality of dependent outcome. 208

209

2. Results

210

Eighteen adolescents with obesity participated in this study. Their mean age was 12.7 ± 1.3 years, 211

body weight was 88.9 ± 23.6 kg (with a BMI of 33.3 ± 6.5 kg/m2 (z-BMI 2.2 ± 0.4), with a percentage of

212

body fat mass of 37.6 ± 5.0 % and a FFM of 53.1 ± 12.5 kg. 213

The adolescents had a V̇O2peak of 21.8 ± 4.6 ml/min/kg. Energy expenditure induced by the exercise

214

(total duration 30 min) was significantly higher compared to the 30-min resting energy expenditure 215

(168.8 ± 43.6 kcal and 46.9 ± 14.9 kcal, respectively; p<0.001). 216

Table 1 details the results related to absolute and relative energy intake. At lunch, absolute ad libitum 217

energy intake was significantly lower in MEAL-90 than MEAL-30 and CON (p<0.05 and p<0.01, 218

respectively) and in MEAL-30 than CON (p<0.05). Dinner ad libitum energy intake was significantly 219

lower in MEAL-90 compared with MEAL-30 (p<0.01) with no difference between the exercise 220

conditions and CON. Total daily absolute ad libitum energy intake was significantly lower in MEAL-90 221

compared with both CON and MEAL-30 (p<0.001). 222

REI at lunch was significantly higher in CON compared with MEAL-30 and MEAL-90 (p<0.05 and 223

p<0.001, respectively) and total REI was significantly higher in CON compared with MEAL-90 (p<0.001). 224

Both lunch (p<0.05) and total REI (p<0.001) were significantly lower in MEAL-90 than MEAL-30. 225

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11 ………Table 1………. 226

The lunch and total absolute intake of protein, fat were significantly lower in MEAL-90 compared with 227

both CON (p<0.01 and p<0.05, respectively) and MEAL-30 (p<0.01 and p<0.05, respectively) while their 228

intake at dinner was significantly lower in MEAL-90 compared with MEAL-30 (p<0.05). The absolute 229

intake of CHO was significantly lower in MEAL-90 compared with CON at lunch (p<0.05) and 230

significantly higher in MEAL-30 compared with CON at dinner (p<0.05). Total absolute CHO intake was 231

only significantly lower in MEAL-90 compared with CON (p<0.05). No significant difference was 232

observed between conditions regarding the relative intake of each macronutrient. Table 2 details 233

these results. 234

………Table 2……… 235

Figure 2 presents the results related to appetite sensations. Fasting hunger, fullness, PFC and DTE did 236

not differ between conditions. After the standardized breakfast, significant differences between 237

conditions were found: hunger and DTE were higher in MEAL-30 than MEAL-90 (p=0.003 and p=0.02), 238

respectively) and CON (p=0.010 and p=0.016, respectively), while PFC was greater in MEAL-30 than 239

MEAL-90 only (p=0.021). Before exercise, hunger was significantly lower during both exercise 240

conditions than during CON (p<0.001 for both). After exercise, this difference remained significant 241

only between CON and MEAL-90 (p=0.004). Immediately before lunch, hunger and PFC were 242

significantly lower in MEAL-30 compared with CON (p=0.036 and p=0.041, respectively). Post-lunch 243

sensations were similar between conditions. Pre-dinner hunger was lower during both exercise 244

conditions compared with CON (p=0.006 for MEAL-30 and p=0.003 for MEAL-90). Pre-dinner fullness 245

was greater in MEAL-30 and MEAL-90 compared with CON (p=0.006 and p=0.003, respectively). 246

Regarding pre-dinner DTE and PFC, only MEAL-90 was significantly lower than CON (p=0.006 and 247

p=0.005, respectively). Concerning the daily AUC (Figure 2), relative to CON, hunger and DTE were 248

significantly lower in MEAL-30 (p=0.019 and p=0.05, respectively) and MEAL-90 (p=0.034 and p=0.031, 249

respectively). 250

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12 ………Figure 2……….. 251

252

As detailed in Table 3, there was a significant condition effect for pre-dinner explicit liking fat bias 253

(p=0.004), with explicit liking for high-fat foods being lower in MEAL-90 compared with both CON 254

(p=0.001) and MEAL-30 (p=0.004). While explicit liking taste bias significantly decreased in response 255

to the lunch meal during the CON condition (p<0.001), this significant meal effect disappeared during 256

both exercise conditions, without a meal x condition interaction. Implicit wanting taste bias 257

significantly increased in response to the lunch test meal during MEAL-90 (p=0.04), and no meal effect 258

was observed in CON and MEAL-30. 259

……….Table 3……….. 260

Discussion

261

The timing of exercise relative to a meal has been recently highlighted for its influence on energy 262

intake and appetite control 1,16, with some recent studies suggesting a better effect of acute exercise

263

performed close to a meal on energy intake and appetite in both adolescents who are lean 19 and

264

adolescents with obesity 20. However these studies did not consider the potential impact of the delay

265

between the exercise and the previous breakfast intake. It has been shown that this delay will impact 266

the metabolic nature of exercise such as the substrates used 21, which might, in turn, differently affect

267

subsequent energy intake 22–24. In that context, the aim of the present study was to investigate the

268

effect of exercise performed at the same delay from breakfast on energy intake, appetite sensations 269

and food reward at the following lunch set either 30 or 90 min after exercise in adolescents with 270

obesity. 271

According to our results, both exercise conditions (MEAL-30 and MEAL-90) led to significantly lower 272

absolute energy intake at lunch compare to CON. This is in line with previous studies in similar 273

populations showing reduced subsequent intake in response to acute exercise set at the same time of 274

the morning 12,14,20,40. Interestingly, absolute energy intake was also significantly lower in MEAL-90

275

compared with MEAL-30, suggesting a greater anorexigenic effect when exercise does not 276

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13 immediately precede the meal. Additionally, total and dinner absolute energy intake were lower 277

during MEAL-90 only, with total daily energy intake reduced by 12% (250 kcal/day) and 16% (352 278

kcal/day) compared with CON and MEAL-30, respectively. These results are reinforced by a lower 279

lunch relative energy intake after MEAL-30 compared with CON and lower lunch and total REI during 280

MEAL-90 compared with both MEAL-30 and CON. Importantly, while most of the available evidence 281

supports the anorexigenic effect of intensive exercise 13,35,41,42, our results reinforce more recent work

282

also observing reduced food intake in response to moderate-to-vigorous exercise in adolescents and 283

children with obesity 40,40.

284

While available evidence indicates the beneficial effect of exercising close to a meal on subsequent 285

energy intake 19,20, our results seem to suggest that more than the exercise-meal delay itself, the

286

interval between the exercise and the following eating episode is of importance. 287

A balanced buffet meal offering several items selected to avoid any over-, under- or occasional-288

consumption (as previously validated 30) was offered to adolescents which provided the opportunity

289

to also assess their macronutrient intake. While none of the relative intake of fat, protein and 290

carbohydrate were found different between conditions, their absolute consumption at lunch was 291

reduced only in MEAL-90 compared with CON, and compared with MEAL-30 for protein and lipid. 292

Interestingly, the absolute intake of carbohydrate at dinner increased in MEAL-30 compared with the 293

two other conditions. The macronutrient responses observed in MEAL-90 seem in line with Albert et 294

al. in lean adolescents 19 and with our previous study in adolescents with obesity 20, showing reduced

295

absolute macronutrient intake after moderate exercise set at the end of the morning. The current 296

study however missed to find similar results in MEAL-30, suggesting here the potential importance of 297

the delay between the exercise and the previous eating episode (breakfast). Indeed, in these previous 298

studies, the appetitive responses to exercise set at different times of the morning, and then at 299

different delays from breakfast, were compared, meaning that despite similar duration, modality and 300

intensity, the exercise was not of similar metabolic and energetic load 21, which might explain our

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14 results. Unfortunately, it was not possible in the present study to measure the substrate oxidation 302

during exercise and at rest. Furthermore, it remains difficult to reach a consensus regarding the effect 303

of acute exercise on macronutrient intake in lean adolescents and in adolescents with obesity based 304

on the available evidence 42.

305

Regarding the adolescents’ subjective appetite sensations, our results show a lower daily (AUC) 306

hunger and desire to eat in both exercise conditions compared with CON. Although pre-lunch hunger 307

and PFC were significantly lower in MEAL-30 compared with CON, which could have contributed to 308

the lower observed ad libitum energy intake, they remained unchanged in MEAL-90 while the 309

decreased food consumption was even more pronounced. This inconsistency between appetite 310

sensations and energy intake reinforce the previously described uncoupling effect of exercise between 311

these sensations and food consumption 43. Interestingly however, post-lunch sensations were

312

identical between exercise conditions, suggesting a similar satiating effect of lunch meals despite 313

lower intakes in MEAL-30 and particularly in MEAL-90, limiting any potential subsequent 314

compensatory responses. This is even reinforced by the significantly reduced food intake observed at 315

dinner in MEAL-90. This is of particular importance since energy deficits, especially when induced by 316

reduced energy intake, have been shown to generate a subsequent compensatory rise in food intake, 317

with physical exercise limiting or avoiding such a compensation 34,44.

318

Some recent studies have highlighted the importance of considering the effect of exercise on food 319

reward to better understand its impact on subsequent energy intake in adolescents with obesity 35.

320

We also assessed whether the liking and wanting for food could be impacted by the delay between 321

eating episodes and exercise in this population. In 2018, Miguet and colleagues observed reduced 322

relative preference for fat and sweet taste, and implicit wanting for high-fat foods (also using the 323

LFPQ) in response to an ad libitum meal set 30 minutes after a 16-minute cycling high intensity interval 324

exercise in a similar population 35. According to the present results, none of the pre or post lunch

325

components of liking and wanting were different between conditions. These results are contradictive 326

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15 with those from Miguet et al. (2018), especially regarding our MEAL-30 condition that had the same 327

delay between the exercise and the meal. However, the exercise intensities were different (high 328

intensity intermittent exercise vs. moderate intensity continuous exercise), reinforcing once more the 329

importance of the exercise intensity in the subsequent control of energy intake. Interestingly, we can 330

see here a significantly lower explicit liking for high-fat food immediately before dinner in MEAL-90 331

compared with the two others, which might contribute to the observed reduced dinner ad libitum 332

food intake. Our results are however also in contradiction with some recently published from our 333

group, showing different food reward responses depending on exercise-meal timing in adolescents 334

with obesity 20. A lower pre-meal explicit liking for high-fat relative to low-fat foods was observed

335

when the adolescents performed 30 min of moderate intensity cycling 60 min before lunch compared 336

with the same exercise performed 180 min before lunch 20. The different LFPQ timing between

MEAL-337

90 and the two other conditions must be considered when interpreting our results. Indeed, food 338

reward was assessed pre- and post- lunch meaning that its delay from exercise was different, which 339

might have affected the results. Although there is a growing interest in the effect of exercise on food 340

reward in this population, evidence remains too limited to draw any conclusion and further studies 341

using standardized designs are needed. 342

The present results must be interpreted in light of some limitations. First, as for the other published 343

studies examining the timing of exercise relative to a meal 16,17,19,20, the lack of direct evaluation of the

344

adolescents’ oxygen consumption and substrate oxidation using indirect calorimeters, as well as the 345

lack of a lean control group to examine the potential weight status effect, are the two main limitations. 346

Although the laboratory-based nature of this work constitutes a strength as it allows a better control 347

of the adolescents’ activity and intake, it might also not be representative of their habitual daily free-348

living setting, such as the school setting for instance, as previously underlined by Mathieu et al. in 349

healthy adolescents 17. Finally, the lack of tracking of the adolescents’ food intake over 24 to 48 hours

350

for practical reasons also limits the interpretation of our results 12.

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16 In line with the present work, another potential important factor, while not addressed in the current 352

study, is the timing of exercise (and food intake) with regards to circadian/diurnal rhythms. Emerging 353

evidence suggests that the timing of exercise 45,46 (and food intake 47,48) impact body weight regulation.

354

Any effects observed from exercise-meal delays may be a result of an interaction with 355

circadian/diurnal oscillations occurring relative to sleep/wake times. Future studies should propose a 356

more complete and integrative exploration of the chronobiologic regulations of energy intake and 357

overall energy metabolism in such adolescents with obesity. Indeed, not only the timings of exercise 358

and /or energy intake should be considered, but also their interactions with the adolescents’ sleep, to 359

better understand and potentially regulate their 24-hour circadian rhythm 49,50. Some key physiological

360

actors of this circadian clock, such as ghrelin and leptin for instance, who are particularly involved in 361

the control of appetite and respondents to sleep and exercise should be mainly considered 51.

362 363

Conclusion

364

To conclude, the present study reinforces the interest in the timing of exercise relative to a meal to 365

affect overall energy balance in youth with obesity; highlighting the importance of the time interval 366

between both the exercise and the previous eating episode, and the exercise and the following meal. 367

According to these results, delaying the timing of the meal after exercise might help reduce energy 368

balance by decreasing ad libitum energy intake without increasing hunger and by improving satiety in 369

adolescents with obesity. Future studies should question the importance of the exercise-meal timing 370

on the longer term. While further acute and chronic studies are needed, these results contribute to 371

the current limited body of evidence in the area and seem important in order to optimize weight loss 372

strategies. 373

374

Conflicts of interest statement

375

None and this research did not receive any specific grant from funding agencies in the public, 376

commercial, or not-for-profit sectors. 377

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17 378

379

Author contributions 380

AF and DT conceived experiments. AF, MM and MB carried out experiments, AF and DT analysed data. 381

KB was involved in writing the paper and all authors had final approval of the submitted and published 382 versions. 383 384 Acknowledgements 385

The authors are grateful to all of the adolescents that participated in the program, and to the Nutrition 386

Obesity Ambulatory Hospital (UGECAM) that provided their generous support. 387

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18

Table legends

389

Table 1: Absolute and Relative Energy Intake in response the three conditions. 390

Table 2: Macronutrient Intake in response the three conditions. 391

Table 3: Pre- and Post-test meal food reward on the three experimental conditions 392

393 394

Figures legends

395

Figure 1 : Study design 396

Figure 2 : Daily appetite sensations and AUC for hunger, fullness, prospective food consumption and 397

desire to eat 398

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19

Table 1: Absolute and Relative Energy Intake in response the three conditions.

400

CON: control condition; MEAL-30: Test meal 30 min after exercise; MEAL-90: Test meal 90 min after exercise; SD: Standard 401

Deviation; ES: Effect Size; *p<0.05 vs. CON ; **p<0.01 vs. CON ; ***p<0.001 vs. CON ; ap<0.05 MEAL-30 vs. MEAL-90 ; 402

bp<0.01 MEAL-30 vs. MEAL-90 ; cp<0.001 MEAL-30 vs. MEAL-90; ES: post hoc effect size 403

404

CON MEAL-30 MEAL-90

p

ES

Mean (SD) Mean (SD) Mean (SD) CON vs. MEAL-30 CON vs. MEAL-90

MEAL-30 vs. MEAL-90 E n e rgy Int ak e (k cal ) Lunch 1380 (185) 1347 (313)* 1168 (234)**a 0.0143 -0.12[-0.60, 0.35] -0.71[-1.19, -0.24] 0.59[0.11, 1.06] Dinner 796 (294) 931 (260) 748 (245)b 0.0363 0.48[0.00, 0.96] -0.20[-0.67, 0.28] 0.68[0.20, 1.15] Total 2175 (330) 2277 (476) 1925 (360)***c 0.0001 0.27[-0.21, 0.74] -0.80[-1.28, -0.33] 1.07[0.59, 1.54] R e lat iv e E ne rg y Int ak e ( k cal ) Lunch 1337 (188) 1172 (313)* 1006 (246)***a 0.0003 -0.56[-1.03, -0.08] -1.08[-1.56, -0.61] 0.52[0.04, 1.00] Total 2119 (332) 2110 (489) 1755 (366)***c <0.0001 -0.11[-0.58, 0.37] -1.16[-1.63, -0.68] 1.06[0.59, 1.54]

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20

Table 2: Macronutrient Intake in response the three conditions.

405

CON MEAL-30 MEAL-90

p

ES

Mean (SD) Mean (SD) Mean (SD)

CON vs. MEAL-30 CON vs. MEAL-90 MEAL-30 vs.

MEAL-90 P rot e ins (g) Lunch 73.8 (11.5) 71.9 (17.2) 60.7 (13.9)**b 0.0059 -0.13[-0.61, 0.34] -0.76[-1.24, -0.29] 0.63[0.15, 1.10] Dinner 42.0 (18.4) 46.8 (14.4) 37.2 (13.2)a 0.1811 0.25[-0.22, 0.73] -0.30[-0.78, 0.17] 0.56[0.08, 1.03] Total 115.9 (22.6) 118.7 (23.8) 98.8 (19.4)***c 0.0007 0.08[-0.40, 0.55] -0.85[-1.32, -0.37] 0.93[0.45, 1.40] P rot e ins (% ) Lunch 21.5 (2.3) 21.4 (3.0) 20.8 (2.3) 0.5108 0.05[-0.42, 0.53] -0.07[-0.55, 0.40] 0.23[-0.25, 0.70] Dinner 20.8 (5.2) 19.9 (3.1) 20.1 (3.6) 0.8811 0.17[-0.31, 0.64] 0.01[-0.46, 0.49] -0.06[-0.53, 0.42] Total 21.3 (2.5) 21.0 (2.0) 20.6 (2.3) 0.6248 0.10[-0.38, 0.58] -0.05[-0.53, 0.42] 0.14[-0.33, 0.62] Li pi ds (g ) Lunch 45.4 (9.6) 45.0 (14.2) 38.1 (12.5)*a 0.0146 -0.06[-0.53, 0.42] -0.54[-1.01, -0.06] 0.48[0.06, 1.01] Dinner 28.8 (19.0) 33.8 (15.1) 26.1 (14.3)a 0.0642 0.33[-0.15, 0.80] -0.18[-0.66, 0.30] 0.51[0.03, 0.98] Total 74.3 (18.0) 78.8 (19.9) 65.8 (19.1)*b 0.0123 0.25[-0.23, 0.72] -0.54[-1.01, -0.06] 0.79[0.31, 1.26] Li pi ds (% ) Lunch 29.8 (5.8) 30.3 (8.0) 29.2 (7.3) 0.1910 0.05[-0.42, 0.53] -0.07[-0.55, 0.40] 0.13[-0.35, 0.60] Dinner 30.0 (12.9) 31.3 (10.6) 29.7 (9.8) 0.0277 0.17[-0.31 0.64] 0.01[-0.46, 0.49] 0.15[-0.32, 0.63] Total 30.7 (5.8) 31.2 (4.8) 30.5 (5.7) 0.9655 0.10[-0.38, 0.58] -0.05[-0.53, 0.42] 0.15[-0.32, 0.63] C HO ( g) Lunch 166.7 (39.4) 160.8 (52.8) 144.2 (34.6)* 0.1649 -0.14[-0.62, 0.33] -0.52[-0.99, -0.04] 0.37[-0.10, 0.85] Dinner 92.8 (31.5) 109.9 (31.5)* 91.9 (29.4)a 0.0269 0.52[0.04, 0.99] -0.036[-0.54, 0.41] 0.58[0.11, 1.06] Total 259.5 (56.1) 270.7 (70.0) 233.9 (49.7)a 0.0751 0.17[-0.31, 0.64] -0.45[-0.92, 0.03] 0.61[0.14, 1.09] C HO ( % ) Lunch 48.0 (7.6) 47.5 (10.5) 49.5 (9.1) 0.2149 0.06[-0.53, 0.42] 0.15[-0.33, 0.62] -0.20[-0.68, 0.27] Dinner 49.7 (15.6) 48.9 (12.4) 50.7 (10.7) 0.0840 -0.01[-0.48, 0.47] 0.13[-0.34, 0.61] -0.14[-0.61, 0.34] Total 47.8 (7.4) 47.4 (6.1) 48.7 (7.3) 0.9547 -0.05[-0.53, 0.42] 0.14[-0.34, 0.61] -0.19[-0.67, 0.28]

CON: control condition; MEAL-30: Test meal 30 minutes after exercise; MEAL-90: Test meal 90 minutes after exercise; SD: 406

Standard Deviation; *p<0.05 vs. CON ; **p<0.01 vs. CON ; ***p<0.001 vs. CON ; ap<0.05 MEAL-30 vs. MEAL-90 ; bp<0.01 407

MEAL-30 vs. MEAL-90 ; cp<0.001 MEAL-30 vs. MEAL-90; ES: Effect Size; CHO: Carbohydrates; ES: post hoc effect size. 408

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21

Table 3: Pre- and Post-test meal food reward on the three experimental conditions

410

CON MEAL-30 MEAL-90

p Interaction time x condition

Mean (SD) Mean (SD) Mean (SD) CON vs. MEAL-30 CON vs. MEAL-90 MEAL-30 vs. MEAL-90 Implicit Wanting Fat Bias Before lunch 22.32 (31.15) 19.96 (33.15) 22.80 (31.68) 0.78 0.99 0.58 0.56 After lunch 20.21 (45.58) 17.63 (48.49) 12.61 (29.50) 0.46 p before vs. after lunch 0.88 0.80 0.90 0.00[-0.48-0.48] -0.13[-0.61-0.34] -0.14[-0.62-0.33] Before dinner 4.37 (64.45) 20.74 (19.89) 14.99 (26.63) 0.49 Taste Bias Before lunch 31.60 (33.67) 34.17 (41.81) 24.90 (32.49) 0.76 0.93 0.14 0.26 After lunch 25.60 (54.02) 27.00 (67.00) 43.59 (30.79) 0.59 p before vs. after lunch 0.69 0.85 0.04 0.02[-0.45-0.50] 0.36[-0.11-0.84] 0.27[-0.20-0.75] Before dinner 38.24 (37.81) 40.40 (40.11) 42.30 (28.12) 0.98 Explicit Liking Fat Bias Before lunch 10.02 (19.71) 12.52 (16.35) 10.53 (19.64) 0.34 0.57 0.77 0.86 After lunch 5.29 (9.39) 5.14 (10.66) 4.08 (9.25) 0.94 p before vs. after lunch 0.27 0.03 0.11 -0.14[-0.61-0.34] -0.07[-0.55-0.40] 0.04[-0.43-0.52] Before dinner 11.35 (19.83) 9.04 (16.34) 2.44 (13.00)***b <0.001 Taste Bias Before lunch 26.18 (20.37) 21.95 (23.03) 20.31 (22.89) 0.82 0.10 0.25 0.74 After lunch 12.78 (19.10) 18.08 (25.78) 14.47 (27.62) 0.73 p before vs. after lunch <0.001 0.38 0.19 0.40[-0.07-0.88] 0.28[-0.19-0.76] -0.08[-0.56-0.40] Before dinner 24.00 (24.58) 21.40 (26.08) 20.76 (28.74) 0.99

CON: control condition; MEAL-30: Test meal 30 min after exercise; MEAL-90: Test meal 90 min after exercise; SD: 411

Standard Deviation; ***p<0.001 vs. CON; bp<0.01 MEAL-30 vs. MEAL-90 ; P values and Effect Size are presented for 412

interactions. 413

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